First Brazilian recommendation on physiotherapy with sensory motor stimulation in newborns and infants in the intensive care unit

Objective To present guidelines on sensory motor stimulation for newborns and infants in the intensive care unit. Methods We employed a mixed methods design with a systematic review of the literature and recommendations based on scientific evidence and the opinions of physiotherapists with neonatal expertise. The research included studies published between 2010 and 2018 in the MEDLINE® and Cochrane databases that included newborns (preterm and term) and infants (between 28 days and 6 months of age) hospitalized in the intensive care unit and submitted to sensory motor stimulation methods. The studies found were classified according to the GRADE score by five physiotherapists in different regions of Brazil and presented at eight Scientific Congresses held to discuss the clinical practice guidelines. Results We included 89 articles to construct the clinical practice guidelines. Auditory, gustatory and skin-to-skin stimulation stand out for enhancing vital signs, and tactile-kinesthetic massage and multisensory stimulation stand out for improving weight or sucking. Conclusion Although all modalities have good ratings for pain or stress control, it is recommended that sensory motor stimulation procedures be tailored to the infant’s specific needs and that interventions and be carried out by expert professionals.


INTRODUCTION
Sensory motor stimulation (SMS) for newborns (preterm or term) and infants in the intensive care unit (ICU) is an early intervention that includes a series of strategies aimed at optimizing neuropsychomotor development (NPMD) by promoting sensory stimuli based on the level of functional development, gestational age (GA) at birth, and weight of this population. (1) The primary aim of SMS is to organize human body systems. i.e., tactile, kinesthetic, vestibular, olfactory, taste, auditory, visual and/or a combination of these. (1) In the ICU, newborns and infants are often in moderately to highly complex clinical situations that may lead to unstable neurological, hemodynamic and cardiorespiratory systems, requiring technical and scientific knowledge when conducting overall assessments of SMS candidates. (2,3) Despite technological advances and multiprofessional efforts, extremely premature (GA < 28 weeks) and extremely low weight (< 1,000g) newborns remain at high risk of death and functional disability (short, mid and long term). Approximately 20% to 50% of survivors are at risk of morbidity, including changes in weight-height growth and NPMD. (2) Sensory motor stimulation facilitates typical NPMD and prevents or minimizes the harmful effects of the ICU environment and interventions on weight-height growth. As such, it can be applied to treat NPMD changes resulting from prematurity, diseases and/or alterations/ complications in the prenatal, perinatal or intranatal period and postdelivery. (4)(5)(6) The aim of the present study is to present clinical practice guidelines on SMS for newborns and infants in the ICU.

Study design
We employed a mixed method design and the following four stages to create this document.
Stage 1 -subject approval for the creation of this document and classification of SMS into the following: Recommendation: the main findings are based on at least one clinical trial, considering scientific evidence on the benefits versus risks to newborns and infants hospitalized in the ICU, viability of comparisons with other intervention options, and confirmation of the reliability of the evidence presented to support the use or rejection of SMS in the clinical practice of physiotherapists.
Guiding question: the PICO domains are considered: P, Patient (newborn or infant); I, Intervention (any SMS intervention); C, Comparison (cross-sectional or prospective longitudinal comparison with itself; with the control, with no intervention or placebo; or with another SMS intervention) and O-Outcome (studies including weight-height outcomes and their indices; improved sleep quality; reduced pain; increase in any NPMD domain; other NPMD-related outcomes -example: arm circumference, bone growth -and weight-height growth).
Stage 2 -a systematic search was conducted of the Medline and Cochrane databases for studies on SMS published between 2010 and 2018. The keywords used included controlled indexers contained in Health Sciences Descriptors (DeCS, available at http://decs.bvs.br/P/ decsweb2014.htm) and/or in Medical Subject Headings (MeSH, available at http://www.ncbi.nlm.nih.gov/entrez/ query.fcgi?db=mesh); a number of free terms related to each SMS modality were also used (see below each subitem of the Recommendations in "descriptors"). The search terms were combined using the Boolean operators "OR" and "AND" and their corresponding Portuguese words. Five specialists conducted the systematic search and assessed the studies independently according to each SMS modality. Disagreements were resolved by common consent of all those present during the discussions and/ or via Skype. The specialists were subdivided into pairs to write a report on the SMS interventions. All specialists were physiotherapists with neonatal expertise (experience ≥ 12 years) in SMS for newborns and infants (up to six months of age) in the ICU.
Stage 3 -the partial data were presented to the public at different pediatric and neonatology congresses, where participants could give their opinions and offer suggestions and comments. The five specialists analyzed the suggestions and comments provided by the public at the aforementioned events and made pertinent changes to the document.
Stage 4 -creation and writing of the document, in line with the three SMS modalities (unimodal and multimodal stimulation and exercises/mobilizations) and the types of interventions found in the literature (Figure 1).

Inclusion and exclusion criteria
Clinical trials that met the following criteria were included: (1) clinical study, controlled or not, comparative or not, randomized or not, or crossover; (2) the study included some type of SMS intervention; (3) study population consisting of newborns and/or infants and

RESULTS
A total of 89 articles were included. The partial data were presented at different pediatric and neonatology congresses: The Brazilian Congress of Intensive Therapy The clinical indicators classified by GRADE are shown in table 1. The tables 1S to 9S in the appendix 1 shows a summary of the data for the studies included.

Unimodal stimulation
Unimodal stimulation includes SMS interventions that provide only one type of sensory stimulation to newborns or infants, in line with the physiological development hierarchy of sensory subsystems, such as tactile→vestibular →taste→olfactory→auditory→visual. (6) Tactile stimulation Recommendation: tactile stimulation is recommended to reduce stress, assessed by urine cortisol level, and applied using the gentle human touch (GHT) intervention; (8) reduce pain intensity, as assessed by the Neonatal Infant Pain Scale (NIPS) and changes in heart rate (HR) and respiratory rate (RR) associated with pain stimuli, using the therapeutic touch (TT) intervention; (9) and improve sleep state, as assessed by the Anderson Behavioral State Scale (ABSS) after the GHT intervention and the Yakson protocol. (10) The clinical indicators classified by GRADE are shown in table 1.

Vestibular stimulation
Recommendation: some functional positioning methods, which can also be used for vestibular stimulation (for example, hammocks, frequently used in the ICU in Brazil), did not exhibit the degree of scientific evidence required for inclusion in unimodal stimulation and were therefore included in multimodal SMS.

Auditory stimulation
Recommendation: auditory stimulation is recommended to increase peripheral capillary oxygen saturation (SpO 2 ) and to reduce HR through exposure to male-sung lullabies; (11) increase SpO 2 through exposure to a Brahms' lullaby or one sung/recorded by the mother; (12) decrease physiological (HR) and behavioral responses (sleep-wake state and facial expressions of pain) during and after pain stimuli; (13,14) decrease resting energy expenditure through exposure to Mozart's music (Mozart effect); (15) lower HR and RR through exposure to lullabies and reduce HR during exposure to Mozart's music; (16) lower HR and RR using three types of interventions (lullabies, heartbeat-like sounds and sounds resembling breathing), better sucking behavior with heartbeat-like sounds and a rise in caloric intake and improved feeding behavior (sucking rate per minute) using lullabies; (17) reduce the frequencies of adverse cardiorespiratory events (18) (defined as the occurrence of apnea > 20 seconds and/or decline in HR to below 100bpm for babies with GA < 34 weeks or below 80bpm for infants > 34 weeks GA), poor sleep-wake cycle, (19) and crying; (20) lower peak HR while feeding, improve sucking, promote faster transition to oral feeding and shorten hospitalization time. (21) One study did not reinforce the beneficial physiological and behavioral effects of lullabies for premature infants. The authors found no significant differences among the intervention (lullaby), placebo and control groups in terms of physiological and behavioral responses. (22) The clinical indicators classified by GRADE are shown in table 1.

Recommendation:
olfactory stimulation is recommended to prevent apnea using stimulation with vanilla fragrance (23) and to reduce pain using odor stimulation with maternal milk. (24) Olfactory stimulation is not recommended to decrease resting energy using vanilla fragrance, (25) and an unfamiliar odor (vanilla) had no noticeable calming effect on healthy full-term newborns subjected to a painful procedure. (26) The clinical indicators classified by GRADE are shown in table 1.

Gustatory stimulation
Recommendation: gustatory stimulation using sensorial saturation, (27) maternal milk, (28) assisted suction, (29,30) and sweetened solutions (glucose, sucralose and dextrose) is recommended to reduce pain. (31-35) When sweetened solutions (glucose, sucralose and dextrose) and placebo stimulations (33-45) were compared, the former decreased pain; only one study compared oral sucrose and EMLA® cream, (37) and the combination of sucrose with EMLA® cream had the greatest analgesic effect. The clinical indicators classified by GRADE are shown in table 1.

Visual stimulation
Recommendation: visual stimulation was included in multimodal SMS rather than unimodal stimulation due to the absence of scientific evidence that met the inclusion criteria of these recommendations.

Multimodal stimulation
Multimodal stimulation includes SMS interventions that combine two or more types of sensory stimuli, as follows: tactile-kinesthetic stimulation, therapeutic massage, skin-to-skin control and multisensory stimulation ( Figure 1).

Kinesthetic tactile stimulation
Recommendation: kinesthetic tactile multimodal stimulation is recommended to improve weight gain and reduce hospitalization time, (46) increase parasympathetic activity during sleep, (47,48) improve muscle strength and bone mineralization, (49) improve motor behavior performance, (50) lower bilirubin levels, (51) favor brain electrical activity maturation, (52) favor more mature motor patterns and more regulated and organized behaviors, (53) improve the motor component and shorten hospitalization time, (54) improve fat deposition in preterm newborns; (55) and contribute to strengthening the immunological system and weight gain. (56,57) The clinical indicators classified by GRADE are shown in table 1.

Massage therapy
Recommendation: multimodal SMS using massage therapy is recommended to increase weight gain, (58)(59)(60) increase the frequency of defecation episodes, (61,62) decrease transcutaneous bilirubin levels, (61-63) reduce pain scores, (64) and raise the state of alertness after massage. (65) The clinical indicators classified by GRADE are shown in table 1.

Skin-to-skin contact
Recommendation: SMS using multimodal stimulation with skin-to-skin contact is recommended for newborns on mechanical ventilation, (66-70) reduces pain during painful procedures, (71-77) alleviates stress, (78,79) controls body temperature, (80) is associated with lower newborn salivary cortisol levels, (79) improves the effectiveness of breastfeeding or weight gain, (81)(82)(83)(84)(85) and decreases cost of hospitalization. (86) One study (84) did not demonstrate a decline in the salivary cortisol levels of preterm newborns; other investigations (85,86) produced no significant evidence in terms of average daily weight gain. The clinical indicators classified by GRADE are shown in table 1.

Multisensory multimodal stimulation
The multisensory stimulation combines different types of stimuli without being necessarily offered simultaneously. Its benefits depend on the maturity of the central nervous system and the sensory subsystems of newborns. (4,87,88) Recommendation: multisensory stimulation is recommended to improve the neuromotor score and muscle tone maturation of preterm newborns by applying the "auditory, tactile, visual and vestibular stimulus -ATVV" protocol, improve behavioral organization, raise the frequency of oral behaviors, extend the time spent in the alertness state, (89,90) improve mother-baby interaction with ATVV (91) and increase weight-height growth. (92) The clinical indicators classified by GRADE are shown in table 1.

Exercises/mobilization
Exercises/mobilization (passive or active-assistive) can be initiated for clinically stable preterm newborns with high risk for bone metabolic disease and GA < 32 weeks and/or birthweight < 1000g. (93,94) The Moyer-Mileur protocol (93) was used in all the studies that met the inclusion criteria of these recommendations.
Recommendation: SMS using mobilizations performed by physiotherapists is recommended to increase weight, height and tibial length; (95) raise the speed of tibial ultrasound propagation; (95,96) increase arm circumference, (97) increase bone formation markers and decrease bone resorption markers. (98,99) The clinical indicators classified by GRADE are shown in table 1.

CONCLUSION
The only sensory motor stimulation modality that has a high degree of scientific certainty was multimodal skinto-skin stimulation, followed by multisensory stimulation. All modalities have good ratings for pain or stress control. Auditory stimulation stands out for enhancing vital signs, and tactile-kinesthetic massage and multisensory multimodal stimulation stand out for improving weight or sucking. It is recommended that sensory motor stimulation procedures be tailored to the infant's specific needs and that interventions and be performed by expert professionals.

AVAILABILITY OF DATA AND MATERIAL
The dataset used and analyzed during the current study is available from the corresponding author on reasonable request. Objetivo: Apresentar as diretrizes para estimulação sensório-motora para recém-nascidos e lactentes em unidade de terapia intensiva.
Conclusão: Embora todas a modalidades tenham boas avaliações para controle da dor ou do estresse, é recomendado que os procedimentos de estimulação sensório-motora sejam adaptados às necessidades específicas da criança, e as intervenções sejam realizadas por profissionais experientes.    (1) Control Group: no intervention (2) Sucking Group: the babies were given pacifiers (3) Lullaby Group: Lullabies were played to the babies through speakers. placed at the infants' feet in the incubator, at 65dB, during force feeding Assessment of peak HR, RR, and SpO 2 before, during and after feeding, body weight, sucking success, transition period to oral feeding, and hospitalization time The pacifier group proceeded to total oral feeding faster, followed by the Lullaby Group Sucking success was achieved by the pacifier group, followed by the Lullaby Group The pacifier group had the shortest hospitalization time, followed by the Lullaby Group There was no difference in RR, SpO 2 and weight between the 3 groups Alipour et al.      Two groups: 23 in the control group 25 submitted to massage therapy using oil on both shoulders starting from the neck with baby in prone position, then the upper back to hip area followed by the upper and lower limbs, one at a time in supine position for 10 minutes, 4 times daily over a period of 28 consecutive days Weight gain; serum triglyceride level; length and head circumference The massage group presented weight gain after 28 days and decreased weight loss within the first 7 days. There was no statistical difference regarding the other outcomes   One group (n = 140): each NB was its own control GA < 37 weeks All NBs were divided into gestational age: 28 -30 weeks (n = 80); 30 -34 weeks (n = 60) and birth weight: 1,000g -1,500 g (n = 88); 1,500 -2,500g (n = 52) Assessment of PIPP during heel puncture, HR, SpO 2 , crying duration and recovery time The effect of skin-to-skin contact was statistically significant in the PTNBs (30 -34 weeks) and very low weight (1,000 -1,500g) groups SpO 2 drop was lower (36% reduction) in the skin-to-skin contact group than in conventional care Crying duration was shorter in the skin-to-skin contact group than in conventional care, with a statistically significant difference PIPP scores were significantly lower with skin-to-skin contact Implementing skin-to-skin contact is a safe method of helping physiological and behavioral stability in PTNBs Evaluate coregulation in salivary cortisol between mother and NB; coregulation defined as progressive reduction in the absolute difference between mother and NB cortisol levels during each 60-minute session of skin-to-skin contact Variable studied: coregulation of salivary cortisol between mother and NB Decreased cortisol levels in mothers and NBs suggesting that skin-to-skin contact caused a decline in stress hormone levels There was no significant difference in coregulation between the groups nonstressful situations, co-regulation in salivary cortisol may not differ based on holding method Evaluate the effects of early skin-toskin contact initiation on exclusive breastfeeding, growth, mortality and morbidity compared to late initiation (during hospitalization and after hospital discharge) in low-weight NBs The early skin-to-skin contact group had higher proportion of exclusive breastfeeding, higher breastfeeding rate during hospitalization, and a higher proportion of exclusive breastfeeding up to one month after hospital discharge The incidence of apnea and recurrent apnea requiring ventilation was significantly reduced in the early skin-toskin contact group There was no significant difference in mortality, morbidity, and growth during hospitalization and after hospital discharge Evaluate the effectiveness of early NB skin-to-skin contact in the Kangaroo unit compared to conventional care in the neonatal unit, in relation to the growth and breastfeeding of very low weight NBs at 40 weeks corrected age. Variables studied: mean weight gain (g/ kg/day) from randomization to corrected term age.
At full-term GA there were no differences between groups regarding mean weight gain (g/kg/day) after randomization and breastfeeding rate. Skin-to-skin contact in the Kangaroo unit is as effective as conventional care at the neonatal unit with no increase in mortality or morbidity in very low weight NBs. The intervention group had faster weight-length gain than the control group GA -gestational age; BW -birth weight; HR -heart rate; SpO 2 -oxygen saturation; FiO 2 -fraction of inspired oxygen; NB -newborn; CPAP -continuous positive airway pressure; TcPCO 2 -transcutaneous carbon dioxide pressure; SSC -skin-to-skin care ; NICU -neonatal intensive care unit; PTNB -preterm newborn; ETT -endotracheal tube; HFNC -high flow nasal cannula; rcO 2 : Regional cerebral oxygenation; HR -heart rate; cFTOE -cerebral fractional tissue oxygen extraction; AT -axillary temperature; RR -respiratory rate; FTNB -full-term newborn; KC -kangoroo care;; PIPP -Premature Infant Pain Profile; KWC -kangorro ward care. ...continuation